53BP1 Alters the Landscape of DNA Rearrangements and Suppresses AID-Induced B Cell Lymphoma

Molecular Cell

Volumn 49, Issue 4, 2013, Pages 623-631

  Jankovic, Mila ^a   Feldhahn, Niklas ^a   Oliveira, Thiago Y ^a,c,d   Silva, Israel T ^a,d   Kieffer Kwon, Kyong Rim ^b   Yamane, Arito ^b   Resch, Wolfgang ^b   Klein, Isaac ^a   Robbiani, Davide F ^a   Casellas, Rafael ^b   Nussenzweig, Michel C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d National Institute of Science and Technology in Stem Cell and Cell Therapy   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; BINDING PROTEIN; PROTEIN P53 BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LYMPHOMA; CANCER CELL; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; MOUSE; NONHUMAN; PROMOTER REGION; SEQUENCE ANALYSIS;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, MAMMALIAN; CYTIDINE DEAMINASE; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENE REARRANGEMENT; GENES, TUMOR SUPPRESSOR; GENOME-WIDE ASSOCIATION STUDY; LYMPHOMA, B-CELL; MICE; MICE, KNOCKOUT; MUTATION; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; TRANSLOCATION, GENETIC;

EID: 84874253686     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.11.029     Document Type: Article

References (63)

1. Anderson L., Henderson C., Adachi Y. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol. Cell. Biol. 2001, 21:1719-1729.
2. Basu U., Meng F.L., Keim C., Grinstein V., Pefanis E., Eccleston J., Zhang T., Myers D., Wasserman C.R., Wesemann D.R., et al. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 2011, 144:353-363.
3. Bignell G.R., Greenman C.D., Davies H., Butler A.P., Edkins S., Andrews J.M., Buck G., Chen L., Beare D., Latimer C., et al. Signatures of mutation and selection in the cancer genome. Nature 2010, 463:893-898.
4. Boeva V., Zinovyev A., Bleakley K., Vert J.-P., Janoueix-Lerosey I., Delattre O., Barillot E. Control-free calling of copy number alterations in deep-sequencing data using GC-content normalization. Bioinformatics 2011, 27:268-269.
5. Bothmer A., Robbiani D.F., Feldhahn N., Gazumyan A., Nussenzweig A., Nussenzweig M.C. 53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination. J. Exp. Med. 2010, 207:855-865.
6. Bouwman P., Aly A., Escandell J.M., Pieterse M., Bartkova J., van der Gulden H., Hiddingh S., Thanasoula M., Kulkarni A., Yang Q., et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 2010, 17:688-695.
7. Bunting S.F., Callén E., Wong N., Chen H.T., Polato F., Gunn A., Bothmer A., Feldhahn N., Fernandez-Capetillo O., Cao L., et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010, 141:243-254.
8. Chaudhuri J., Khuong C., Alt F.W. Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature 2004, 430:992-998.
9. Chiarle R., Zhang Y., Frock R.L., Lewis S.M., Molinie B., Ho Y.J., Myers D.R., Choi V.W., Compagno M., Malkin D.J., et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 2011, 147:107-119.
10. Difilippantonio S., Gapud E., Wong N., Huang C.Y., Mahowald G., Chen H.T., Kruhlak M.J., Callen E., Livak F., Nussenzweig M.C., et al. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 2008, 456:529-533.
11. Di Noia J.M., Williams G.T., Chan D.T., Buerstedde J.M., Baldwin G.S., Neuberger M.S. Dependence of antibody gene diversification on uracil excision. J. Exp. Med. 2007, 204:3209-3219.
12. DiTullio R.A., Mochan T.A., Venere M., Bartkova J., Sehested M., Bartek J., Halazonetis T.D. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 2002, 4:998-1002.
13. Fernandez-Capetillo O., Chen H.T., Celeste A., Ward I., Romanienko P.J., Morales J.C., Naka K., Xia Z., Camerini-Otero R.D., Motoyama N., et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 2002, 4:993-997.
14. Franco S., Gostissa M., Zha S., Lombard D.B., Murphy M.M., Zarrin A.A., Yan C., Tepsuporn S., Morales J.C., Adams M.M., et al. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol. Cell 2006, 21:201-214.
15. Gostissa M., Alt F.W., Chiarle R. Mechanisms that promote and suppress chromosomal translocations in lymphocytes. Annu. Rev. Immunol. 2011, 29:319-350.
16. Hakim O., Resch W., Yamane A., Klein I., Kieffer-Kwon K.R., Jankovic M., Oliveira T., Bothmer A., Voss T.C., Ansarah-Sobrinho C., et al. DNA damage defines sites of recurrent chromosomal translocations in B lymphocytes. Nature 2012, 484:69-74.
17. Helmink B.A., Tubbs A.T., Dorsett Y., Bednarski J.J., Walker L.M., Feng Z., Sharma G.G., McKinnon P.J., Zhang J., Bassing C.H., Sleckman B.P. H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes. Nature 2011, 469:245-249.
18. Jankovic M., Nussenzweig A., Nussenzweig M.C. Antigen receptor diversification and chromosome translocations. Nat. Immunol. 2007, 8:801-808.
19. Kalhor R., Tjong H., Jayathilaka N., Alber F., Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 2012, 30:90-98.
20. Keane T.M., Goodstadt L., Danecek P., White M.A., Wong K., Yalcin B., Heger A., Agam A., Slater G., Goodson M., et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 2011, 477:289-294.
21. Klein I.A., Resch W., Jankovic M., Oliveira T., Yamane A., Nakahashi H., Di Virgilio M., Bothmer A., Nussenzweig A., Robbiani D.F., et al. Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 2011, 147:95-106.
22. Krzywinski M., Schein J., Birol I., Connors J., Gascoyne R., Horsman D., Jones S.J., Marra M.A. Circos: an information aesthetic for comparative genomics. Genome Res. 2009, 19:1639-1645.
23. Kumar-Sinha C., Tomlins S.A., Chinnaiyan A.M. Recurrent gene fusions in prostate cancer. Nat. Rev. Cancer 2008, 8:497-511.
24. Küppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat. Rev. Cancer 2005, 5:251-262.
25. Lee A.C., Fernandez-Capetillo O., Pisupati V., Jackson S.P., Nussenzweig A. Specific association of mouse MDC1/NFBD1 with NBS1 at sites of DNA-damage. Cell Cycle 2005, 4:177-182.
26. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
27. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
28. Liu M., Duke J.L., Richter D.J., Vinuesa C.G., Goodnow C.C., Kleinstein S.H., Schatz D.G. Two levels of protection for the B cell genome during somatic hypermutation. Nature 2008, 451:841-845.
29. Mahowald G.K., Baron J.M., Mahowald M.A., Kulkarni S., Bredemeyer A.L., Bassing C.H., Sleckman B.P. Aberrantly resolved RAG-mediated DNA breaks in Atm-deficient lymphocytes target chromosomal breakpoints in cis. Proc. Natl. Acad. Sci. USA 2009, 106:18339-18344.
30. Morales J.C., Franco S., Murphy M.M., Bassing C.H., Mills K.D., Adams M.M., Walsh N.C., Manis J.P., Rassidakis G.Z., Alt F.W., Carpenter P.B. 53BP1 and p53 synergize to suppress genomic instability and lymphomagenesis. Proc. Natl. Acad. Sci. USA 2006, 103:3310-3315.
31. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
32. Muto T., Okazaki I.M., Yamada S., Tanaka Y., Kinoshita K., Muramatsu M., Nagaoka H., Honjo T. Negative regulation of activation-induced cytidine deaminase in B cells. Proc. Natl. Acad. Sci. USA 2006, 103:2752-2757.
33. Noon A.T., Shibata A., Rief N., Löbrich M., Stewart G.S., Jeggo P.A., Goodarzi A.A. 53BP1-dependent robust localized KAP-1 phosphorylation is essential for heterochromatic DNA double-strand break repair. Nat. Cell Biol. 2010, 12:177-184.
34. Nussenzweig A., Nussenzweig M.C. Origin of chromosomal translocations in lymphoid cancer. Cell 2010, 141:27-38.
35. Okazaki I.M., Kotani A., Honjo T. Role of AID in tumorigenesis. Adv. Immunol. 2007, 94:245-273.
36. Oliveira T.Y., Resch W., Jankovic M., Casellas R., Nussenzweig M.C., Klein I.A. Translocation capture sequencing: a method for high throughput mapping of chromosomal rearrangements. J. Immunol. Methods 2012, 375:176-181.
37. Pasqualucci L., Neumeister P., Goossens T., Nanjangud G., Chaganti R.S., Küppers R., Dalla-Favera R. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 2001, 412:341-346.
38. Pavri R., Nussenzweig M.C. AID targeting in antibody diversity. Adv. Immunol. 2011, 110:1-26.
39. Pavri R., Gazumyan A., Jankovic M., Di Virgilio M., Klein I., Ansarah-Sobrinho C., Resch W., Yamane A., Reina San-Martin B., Barreto V., et al. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 2010, 143:122-133.
40. Potter M. Neoplastic development in plasma cells. Immunol. Rev. 2003, 194:177-195.
41. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
42. Quinlan A.R., Clark R.A., Sokolova S., Leibowitz M.L., Zhang Y., Hurles M.E., Mell J.C., Hall I.M. Genome-wide mapping and assembly of structural variant breakpoints in the mouse genome. Genome Res. 2010, 20:623-635.
43. Ramiro A.R., Jankovic M., Callen E., Difilippantonio S., Chen H.T., McBride K.M., Eisenreich T.R., Chen J., Dickins R.A., Lowe S.W., et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 2006, 440:105-109.
44. Rappold I., Iwabuchi K., Date T., Chen J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 2001, 153:613-620.
45. Revy P., Muto T., Levy Y., Geissmann F., Plebani A., Sanal O., Catalan N., Forveille M., Dufourcq-Labelouse R., Gennery A., et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 2000, 102:565-575.
46. Robbiani D.F., Bothmer A., Callen E., Reina-San-Martin B., Dorsett Y., Difilippantonio S., Bolland D.J., Chen H.T., Corcoran A.E., Nussenzweig A., Nussenzweig M.C. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 2008, 135:1028-1038.
47. Robbiani D.F., Bunting S., Feldhahn N., Bothmer A., Camps J., Deroubaix S., McBride K.M., Klein I.A., Stone G., Eisenreich T.R., et al. AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol. Cell 2009, 36:631-641.
48. Schoenfelder S., Sexton T., Chakalova L., Cope N.F., Horton A., Andrews S., Kurukuti S., Mitchell J.A., Umlauf D., Dimitrova D.S., et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 2010, 42:53-61.
49. Schultz L.B., Chehab N.H., Malikzay A., Halazonetis T.D. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 2000, 151:1381-1390.
50. Shaffer A.L., Rosenwald A., Staudt L.M. Lymphoid malignancies: the dark side of B-cell differentiation. Nat. Rev. Immunol. 2002, 2:920-932.
51. Shen H.M., Bozek G., Pinkert C.A., McBride K., Wang L., Kenter A., Storb U. Expression of AID transgene is regulated in activated B cells but not in resting B cells and kidney. Mol. Immunol. 2008, 45:1883-1892.
52. Sproul D., Gilbert N., Bickmore W.A. The role of chromatin structure in regulating the expression of clustered genes. Nat. Rev. Genet. 2005, 6:775-781.
53. Stavnezer J., Guikema J.E., Schrader C.E. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 2008, 26:261-292.
54. Stephens P.J., McBride D.J., Lin M.L., Varela I., Pleasance E.D., Simpson J.T., Stebbings L.A., Leroy C., Edkins S., Mudie L.J., et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009, 462:1005-1010.
55. Storb U., Shen H.M., Longerich S., Ratnam S., Tanaka A., Bozek G., Pylawka S. Targeting of AID to immunoglobulin genes. Adv. Exp. Med. Biol. 2007, 596:83-91.
56. Symington L.S., Gautier J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 2011, 45:247-271.
57. Takeyama K., Monti S., Manis J.P., Dal Cin P., Getz G., Beroukhim R., Dutt S., Aster J.C., Alt F.W., Golub T.R., Shipp M.A. Integrative analysis reveals 53BP1 copy loss and decreased expression in a subset of human diffuse large B-cell lymphomas. Oncogene 2008, 27:318-322.
58. Ward I.M., Minn K., van Deursen J., Chen J. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 2003, 23:2556-2563.
59. Ward I.M., Difilippantonio S., Minn K., Mueller M.D., Molina J.R., Yu X., Frisk C.S., Ried T., Nussenzweig A., Chen J. 53BP1 cooperates with p53 and functions as a haploinsufficient tumor suppressor in mice. Mol. Cell. Biol. 2005, 25:10079-10086.
60. Yamane A., Resch W., Kuo N., Kuchen S., Li Z., Sun H.W., Robbiani D.F., McBride K., Nussenzweig M.C., Casellas R. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat. Immunol. 2011, 12:62-69.
61. Yamane A., Robbiani D.F., Resch W., Bothmer A., Nakahashi H., Oliveira T., Rommel P.C., Brown E.J., Nussenzweig A., Nussenzweig M.C., Casellas R. RPA Accumulation during Class Switch Recombination Represents 5'-3' DNA-End Resection during the S-G2/M Phase of the Cell Cycle. Cell Rep. 2013, Published online January 3, 2013. 10.1016/j.celrep.2012.12.006.
62. Zhang Y., Gostissa M., Hildebrand D.G., Becker M.S., Boboila C., Chiarle R., Lewis S., Alt F.W. The role of mechanistic factors in promoting chromosomal translocations found in lymphoid and other cancers. Adv. Immunol. 2010, 106:93-133.
63. Ziv Y., Bielopolski D., Galanty Y., Lukas C., Taya Y., Schultz D.C., Lukas J., Bekker-Jensen S., Bartek J., Shiloh Y. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 2006, 8:870-876.